Visual recognition of social signals by a tecto-thalamic neural circuit

Abstract

Social affiliation emerges from individual-level behavioral rules that are driven by conspecific signals. Long-distance attraction and short-distance repulsion, for example, are rules that jointly set a preferred inter-animal distance in swarms. However, little is known about their perceptual mechanisms and executive neuronal circuits. Here we trace the neuronal response to self-like biological motion (BM), a visual trigger for affiliation in developing zebrafish. Unbiased activity mapping and targeted volumetric two-photon calcium imaging revealed 19 activity hotspots distributed throughout the brain and clustered BM-tuned neurons in a multimodal, socially activated nucleus of the dorsal thalamus (DT). Individual DT neurons encode fish-like local acceleration but are insensitive to global or continuous motion. Electron microscopic reconstruction of DT neurons revealed synaptic input from the optic tectum (TeO/superior colliculus) and projections into nodes of the conserved social behavior network. Chemogenetic ablation of the TeO selectively disrupted DT responses to BM and social attraction without affecting short-distance repulsion. Together, we discovered a tecto-thalamic pathway that drives a core network for social affiliation. Our findings provide an example of visual social processing, and dissociate neuronal control of attraction from repulsion during affiliation, thus revealing neural underpinnings of collective behavior.

Quantity as a Fish Views It: Behavior and Neurobiology

“…Therefore, pth2 expression seems specific for mechanical stimulation and strongly tracks the group size of conspecifics. Remarkably, these pth2 expressing neurons overlap with the bout preference cells in the dorsal thalamus (Kappel et al, 2021). This might suggest the dorsal thalamus as a possible multisensory area integrating sensory signals of conspecifics.…”

“…A specific visual circuit involved in the selection of larvae characteristic swim kinetics (bout-like acceleration) was found in juveniles of 21 dpf (Kappel et al, 2021, see Figure 2). Global activity maps by c-fos in situ hybridization chain reaction (HRC) revealed a cluster of brain areas whose activity was modulated by virtual and real conspecifics.…”

“…(C) Left: black dots with bout-like motion elicited shoaling behavior in juvenile zebrafish, while continuously moving dots were considered not attractive (Larsch and Baier, 2018). Right: Connectivity patterns of dorsal thalamus where Kappel et al (2021) found a cluster of neurons selective for bout swim. Rth, rostral thalamus; POA, preoptic area; CMid, caudal midbrain; DT, dorsal thalamus; OT, optic tectum; Hyp, hypothalamus.…”

A single-cell resolution gene expression atlas of the larval zebrafish brain

“…Recent developments of FISH techniques, such as RNAscope, MERFISH and HCR (Chen et al, 2015; Choi et al, 2018; Wang et al, 2012), offer single RNA molecule detection and multiplexing in vivo. We chose HCR, because the staining protocol is easily implemented in larval and juvenile fish (Choi et al, 2018; Kappel et al, 2021) and is suitable for registration into a common 3D reference (Kappel et al, 2021; Lovett-Barron et al, 2020). HCR technology enables multiplexed FISH of up to 5 probe sets per round of staining with different fluorophores (Choi et al, 2018).…”

Wild animals suppress the spread of socially-transmitted misinformation

“…However, in many situations such as in crowds [21], automobile traffic [22], bird flocks [1,20], and animal feeding aggregations [14,23], decisions must be made rapidly [19,22] in large or ephemeral [24] collectives, where using foreknowledge of the reliability of all senders is impossible. Behavioural and neurophysiological studies suggest that relatively simple behavioural strategies control decision-making in many such settings [21][22][23][25][26][27]]. Yet, whether these strategies somehow account for the possibility of exposure to misinformation is unknown.…”